Evolutionary islands in the Andes: Persistence and isolation explain high endemism in Andean dry tropical forests

Journal of Biogeography

Volumn 39, Issue 5, 2012, Pages 884-900

  Särkinen, Tiina ^a,b,f   Pennington, R Toby ^a   Lavin, Matt ^c   Simon, Marcelo F ^d   Hughes, Colin E ^b,e  

^a ROYAL BOTANIC GARDEN EDINBURGH   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MONTANA STATE UNIVERSITY   (United States)

^d EMBRAPA RECURSOS GENÉTICOS E BIOTECNOLOGIA   (Brazil)

^e UNIVERSITY OF ZURICH   (Switzerland)

^f DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

Author keywords

Andean uplift; Biodiversity hotspot; Island biogeography; Molecular dating; Phylogenetic niche conservatism; Seasonally dry tropical forest; Species diversification

Indexed keywords

BIODIVERSITY; BIOGEOGRAPHY; BIOME; CALIBRATION; CLADISTICS; DATING METHOD; ENDEMIC SPECIES; HETEROGENEITY; HOT SPOT; LEGUME; MOLECULAR ANALYSIS; NICHE; PHYLOGENY; SEASONALITY; TROPICAL FOREST; UPLIFT;

ANDENES; ANDOYA; NORWAY; VESTERALEN;

AMICIA; COURSETIA; CYATHOSTEGIA; MIMOSA;

EID: 84859849616     PISSN: 03050270     EISSN: 13652699     Source Type: Journal    
DOI: 10.1111/j.1365-2699.2011.02644.x     Document Type: Article

References (74)

1. Bailey, C.D., Carr, T.G., Harris, S.A. & Hughes, C.E. (2003) Characterization of angiosperm nrDNA polymorphism, paralogy and pseudogenes. Molecular Phylogenetics and Evolution, 29, 435-455.
2. Barke, R. & Lamb, S. (2006) Late Cenozoic uplift of the Eastern Cordillera, Bolivian Andes. Earth and Planetary Science Letters, 249, 350-367.
3. Barraclough, T. (2010) Evolving entities: towards a unified framework for understanding diversity at the species and higher levels. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 1801-1813.
4. Bletter, N., Janovec, J., Brosi, B. & Daly, D.C. (2004) A digital base map for studying the Neotropical flora. Taxon, 53, 469-477.
5. Brako, L. & Zarucchi, J.L. (1993) Catalogue of the flowering plants and gymnosperms of Peru. Missouri Botanical Garden, St Louis, MO.
6. Burnham, R.J. (1995) A new species of winged fruit from the Miocene of Ecuador: Tipuana ecuatoriana. American Journal of Botany, 82, 1599-1607.
7. Burnham, R.J. & Carranco, N.L. (2004) Miocene winged fruits of Loxopterygium (Anacardiaceae) from the Ecuadorian Andes. American Journal of Botany, 91, 1767-1773.
8. Crisp, M.C., Cook, L. & Steane, D. (2004) Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities? Philosophical Transactions of the Royal Society B: Biological Sciences, 359, 1551-1571.
9. Crisp, M.D., Arroyo, M., Cook, L., Gandolfo, M., Jordan, G., McGlone, M., Weston, P., Westoby, M., Wilf, P. & Linder, H.P. (2009) Phylogenetic biome conservatism on a global scale. Nature, 458, 754-758.
10. Cuatrecasas, J. (1979) Growth forms of the Espeletiinae and their correlation to vegetation types of the high tropical Andes. Tropical botany (ed. by K. Larsen and L.B. Holm-Nielsen ), pp. 397-410. Academic Press, London.
11. Donoghue, M.J. (2008) A phylogenetic perspective on the distribution of plant diversity. Proceedings of the National Academy of Sciences USA, 105, 11549-11555.
12. Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
13. Drummond, A.J., Ho, S.Y.W., Phillips, M.J. & Rambaut, A. (2006) Relaxed phylogenetics and dating with confidence. PloS Biology, 4, e88.
14. Edwards, D. & Hawkins, J.A. (2007) Are Cape floral clades the same age? Contemporaneous origins of two lineages in the genistoids s.l. (Fabaceae). Molecular Phylogenetics and Evolution, 45, 952-970.
15. Ehlers, T.A. & Poulsen, C.J. (2009) Influence of Andean uplift on climate and paleoaltimetry estimates. Earth and Planetary Science Letters, 281, 238-248.
16. Francisco, S.M., Faria, C., Lengkeek, W., Vieira, M.N., Velasco, E.M. & Almada, V.C. (2011) Phylogeography of the shanny Lipophrys pholis (Pisces: Blenniidae) in the NE Atlantic records signs of major expansion event older than the last glaciation. Journal of Experimental Marine Biology and Ecology, 403, 14-20.
17. Funk, D.J. & Omland, K.E. (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution and Systematics, 34, 397-423.
18. Garzione, C.N., Hoke, G.D., Libarkin, J.C., Withers, S., MacFadden, B., Eiler, J., Ghosh, P. & Mulch, A. (2008) Rise of the Andes. Science, 320, 1304-1307.
19. Gentry, A.H. (1982) Neotropical floristic diversity: phytogeographical connections between Central and South America, Pleistocene climatic fluctuations, or an accident of the Andean orogeny? Annals of the Missouri Botanical Garden, 69, 557-593.
20. Ghalambor, C.K., Huey, R.B., Martin, P.R., Tewksbury, J.J. & Wang, G. (2006) Are mountain passes higher in the tropics? Janzen's hypothesis revisited. Integrative and Comparative Biology, 46, 5-17.
21. 18O bonds in paleosol carbonates. Science, 311, 511-515.
22. Goslee, S.C. & Urban, D.L. (2007) The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software, 22, 1-19.
23. van der Hammen, T. & Cleef, A.M. (1986) Development of the high Andean paramo flora and vegetation. High altitude tropical biogeography (ed. by F. Vuilleumier and M. Monasterio ), pp. 153-201. Oxford University Press, New York.
24. Hartley, A.J. (2003) Andean uplift and climate change. Journal of the Geological Society, London, 160, 7-10.
25. Hartley, A.J., Chong, G., Houston, J. & Mather, A.E. (2005) 150million years of climatic stability: evidence from the Atacama Desert, northern Chile. Journal of the Geological Society, London, 162, 421-424.
26. Hooghiemstra, H. & Cleef, A.M. (1995) Pleistocene climatic change and environmental and generic dynamics in the north Andean montane forest and páramo. Biodiversity and conservation of Neotropical montane forests (ed. by S.P. Churchill, H. Balslev, E. Forero and J.L. Luteyn ), pp. 35-49. New York Botanical Garden, New York.
27. Hooghiemstra, H., Wijninga, V.M. & Cleef, A.M. (2006) The paleobotanical record of Colombia: implications for biogeography and biodiversity. Annals of the Missouri Botanical Garden, 93, 297-325.
28. Houston, J. & Hartley, A.J. (2003) The central Andean west-slope rainshadow and its potential contribution to the origin of hyper-aridity in the Atacama desert. International Journal of Climatology, 23, 1453-1464.
29. Hughes, C.E. & Eastwood, R. (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proceedings of the National Academy of Sciences USA, 103, 10334-10339.
30. Janzen, D.H. (1967) Why mountain passes are higher in the tropics. The American Naturalist, 101, 233-249.
31. Jørgensen, P.M., Neill, D.A. & León-Yánez, S. (1999) Catalogue of the vascular plants of Ecuador. Missouri Botanical Garden, St Louis, MO.
32. Killeen, T.J., Douglas, M., Consiglio, T., Jørgensen, P.M. & Mejia, J. (2007) Dry spots and wet spots in the Andean hotspot. Journal of Biogeography, 34, 1357-1373.
33. Kreft, H. & Jetz, W. (2007) Global patterns and determinants of vascular plant diversity. Proceedings of the National Academy of Sciences USA, 104, 5925-5930.
34. Kroonenberg, S.B., Bakker, J.G.M. & van der Wiel, A.M. (1990) Late Cenozoic uplift and paleogeography of the Colombian Andes: constraints on the development of high-Andean biota. Geologie en Mijnbouw, 69, 279-290.
35. Lavin, M. (1988) Systematics of Coursetia (Leguminosae-Papilionoideae). Systematic Botany Monographs, 21, 1-167.
36. Lavin, M. & Beyra Matos, A. (2008) The impact of ecology and biogeography on legume diversity, endemism, and phylogeny in the Caribbean region: a new direction in historical biogeography. The Botanical Review, 74, 178-196.
37. Lavin, M., Wojciechowski, M.F., Gasson, P., Hughes, C.E. & Wheeler, E. (2003) Phylogeny of robinioid legumes (Fabaceae) revisited: Coursetia and Gliricidia re-circumscribed, and a biogeographical appraisal of the Caribbean endemics. Systematic Botany, 28, 387-409.
38. Linares-Palomino, R. (2006) Phytogeography and floristics of seasonally dry tropical forests in Peru. Neotropical savannas and seasonally dry forests (ed. by R.T. Pennington, G.P. Lewis and J.A. Ratter ), pp. 257-280. CRC Press, Boca Raton, FL.
39. Linares-Palomino, R. & Kessler, M. (2008) The role of dispersal ability, climate and spatial separation in shaping biogeographical patterns of phylogenetically distant plant groups in seasonally dry Andean forests of Bolivia. Journal of Biogeography, 36, 280-290.
40. Linares-Palomino, R., Oliveira-Filho, A.T. & Pennington, R.T. (2011) Neotropical seasonally dry forests: diversity, endemism and biogeography of woody plants. Seasonally dry tropical forests: ecology and conservation (ed. by R. Dirzo, H. Mooney, G. Ceballos and H. Young ), pp. 3-21. Island Press, Washington, DC.
41. Linder, H.P. (2005) Evolution of diversity: the Cape flora. Trends in Plant Science, 10, 536-541.
42. Magallón, S. & Sanderson, M.J. (2001) Absolute diversification rates in angiosperm clades. Evolution, 55, 1762-1780.
43. Missouri Botanical Garden (2009) Tropicos. Missouri Botanical Garden, St Louis, MO. Available at: (accessed 20 November 2009).
44. Mittermeier, R.A., Gil, P.R., Hoffman, M., Pilgrim, J., Brooks, T., Mittermeier, C.G., Lamoreux, J. & de Fonseca, G.A.B. (2005) Hotspots revisited: Earth's biologically richest and most endangered terrestrial ecoregions. University of Chicago Press, Chicago, IL.
45. Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853-858.
46. Neigel, J.E. (1997) A comparison of alternative strategies for estimating gene flow from genetic markers. Annual Review of Ecology and Systematics, 28, 105-128.
47. Olson, D.M. & Dinerstein, E. (2002) The Global 200: priority ecoregions for global conservation. Annals of the Missouri Botanical Garden, 89, 199-224.
48. Orme, C.D.L., Davies, R.G., Burgess, M., Eigenbrod, F., Pickup, N., Olson, V.A., Webster, A.J., Ding, T.-S., Rasmussen, P.C., Ridgely, R.S., Stattersfield, A.J., Bennett, P.M., Blackburn, T.M., Gaston, K.J. & Owens, I.P.F. (2005) Global hotspots of species richness are not congruent with endemism or threat. Nature, 436, 1016-1019.
49. Pennington, R.T., Prado, D.A. & Pendry, C. (2000) Neotropical seasonally dry forests and Pleistocene vegetation changes. Journal of Biogeography, 27, 261-273.
50. Pennington, R.T., Lavin, M., Prado, D.E., Pendry, C.A., Pell, S.K. & Butterworth, C.A. (2004) Historical climate change and speciation: neotropical seasonally dry forest plants show patterns of both Tertiary and Quaternary diversification. Philosophical Transactions of the Royal Society B: Biological Sciences, 359, 515-537.
51. Pennington, R.T., Lavin, M. & Oliveira-Filho, A. (2009) Woody plant diversity, evolution, and ecology in the tropics: perspectives from seasonally dry tropical forests. Annual Review of Ecology, Evolution, and Systematics, 40, 437-457.
52. Pennington, R.T., Lavin, M., Särkinen, T., Lewis, G.P., Klitgaard, B.B. & Hughes, C.E. (2010) Contrasting plant diversification histories within the Andean biodiversity hotspot. Proceedings of the National Academy of Sciences USA, 107, 13783-13787.
53. Pennington, R.T., Daza, A. & Lavin, M. (2011) Poissonia eriantha (Leguminosae) from Cuzco, Peru: an overlooked species underscores a pattern of narrow endemism common to seasonally dry Neotropical vegetation. Systematic Botany, 36, 59-68.
54. Qian, H. & Ricklefs, R.E. (2000) Large-scale processes and the Asian bias in species diversity of temperate plants. Nature, 407, 180-182.
55. de Queiroz, L.P. & Lavin, M. (2011) Coursetia (Leguminosae) from eastern Brazil: nuclear ribosomal and chloroplast DNA sequence analysis reveal the monophyly of three caatinga-inhabiting species. Systematic Botany, 36, 69-79.
56. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: .
57. Rauscher, J.T. (2002) Molecular phylogenetics of the Espeletia complex (Asteraceae): evidence from nrDNA ITS sequences on the closest relatives of an Andean adaptive radiation. American Journal of Botany, 89, 1074-1084.
58. Ruggiero, A. & Hawkins, B.A. (2008) Why do mountains support so many species of birds? Ecography, 31, 306-315.
59. Särkinen, T.E., Marcelo-Peña, J.L., Yomona, A.D., Simon, M.F., Pennington, R.T. & Hughes, C.E. (2011) Underestimated endemic species diversity in the dry inter-Andean valley of the Río Marañón, northern Peru: an example from Mimosa (Leguminosae, Mimosoideae). Taxon, 60, 139-150.
60. Sauquet, H., Weston, P.H., Anderson, C.L., Barker, N.P., Cantrill, D.J., Mast, A.R. & Savolainen, V. (2009) Contrasted patterns of hyperdiversification in Mediterranean hotspots. Proceedings of the National Academy of Sciences USA, 106, 221-225.
61. Schildgen, T.F., Hodges, K.V., Whipple, K.X., Reiners, P.W. & Pringle, M.S. (2007) Uplift of the western margin of the Andean plateau revealed from canyon incision history, southern Peru. Geology, 35, 523-526.
62. Schrire, B.D., Lavin, M., Barker, N.P. & Forest, F. (2009) Phylogeny of the tribe Indigofereae (Leguminosae-Papilionoideae): geographically structured more in succulent-rich and temperate settings than in grass-rich environments. American Journal of Botany, 96, 816-852.
63. Sempere, T., Folguera, A. & Gerbault, M. (2008) New insights into Andean evolution: an introduction to contributions from the 6th ISAG symposium (Barcelona, 2005). Tectonophysics, 459, 1-13.
64. Simon, M.F., Grether, R., de Queiroz, L., Skema, C., Pennington, R.T. & Hughes, C.E. (2009) Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proceedings of the National Academy of Sciences USA, 106, 20359-20364.
65. Syring, J., Farrell, K., Businský, R., Cronn, R. & Liston, A. (2007) Widespread genealogical nonmonophyly in species of Pinus subgenus Strobus. Systematic Biology, 56, 163-181.
66. Thouret, J.-C., Wörner, G., Gunnell, Y., Singer, B., Zhang, X. & Souriot, T. (2007) Geochronologic and stratigraphic constraints on canyon incision and Miocene uplift of the Central Andes in Peru. Earth and Planetary Science Letters, 263, 151-166.
67. Trenél, P., Hansen, M.M., Normand, S. & Borchsenius, F. (2008) Landscape genetics, historical isolation and cross-Andean gene flow in the wax palm, Ceroxylon echinulatum (Arecaceae). Molecular Ecology, 17, 3528-3540.
68. Tye, A. (2000) Las plantas vasculares endemicas de Galapagos. Libro rojo de las plantas endemicas del Ecuador 2000 (ed. by R. Valencia, N. Pitman, S. Leon-Yanez and P.M. Jorgensen ), pp. 24-28. Herbario QCA, Pontificia Universidad Catolica del Ecuador, Quito.
69. Verboom, G.A., Archibald, J.K., Bakker, F.T., Bellstedt, D.U., Conrad, F., Dreyer, L.L., Forest, F., Galley, C., Goldblatt, P., Henning, J.F., Mummenhoff, K., Linder, H.P., Muasya, A.M., Oberlander, K.C., Savolainen, V., Snijman, D.A., van der Niet, T. & Nowell, T.L. (2009) Origin and diversification of the Greater Cape flora: ancient species repository, hot-bed of recent radiation, or both? Molecular Phylogenetics and Evolution, 51, 44-53.
70. Villaseñor, J.L., Maeda, P., Rosell, J.A. & Ortiz, E. (2007) Plant families as predictors of plant biodiversity in Mexico. Diversity and Distributions, 13, 871-876.
71. Whittaker, R.J. & Fernández-Palacios, J.M. (2007) Island biogeography, ecology, evolution, and conservation. Oxford University Press, Oxford.
72. Whittaker, R.J., Triantis, K.A. & Ladle, R.J. (2008) A general dynamic theory of oceanic island biogeography. Journal of Biogeography, 35, 977-994.
73. Wright, S. (1943) Isolation by distance. Genetics, 28, 114-138.
74. Yesson, C., Brewer, P.W., Sutton, T., Caithness, N. & Pahwa, J.S. (2007) How global is the Global Biodiversity Information Facility? PLoS ONE, 2, e1124.